The Ku80 Carboxy Terminus Stimulates Joining and Artemis-Mediated Processing of DNA Ends

REFERENCES

• Chan, D. W., B. P. Chen, S. Prithivirajsingh, A. Kurimasa, M. D. Story, J. Qin, and D. J. Chen. 2002. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev. 16:2333–2338.
   PubMed Web of Science ®Google Scholar
• Chan, D. W., C. H. Mody, N. S. Ting, and S. P. Lees-Miller. 1996. Purification and characterization of the double-stranded DNA-activated protein kinase, DNA-PK, from human placenta. Biochem. Cell Biol. 74:67–73.
   PubMedGoogle Scholar
• Chappell, C., L. A. Hanakahi, F. Karimi-Busheri, M. Weinfeld, and S. C. West. 2002. Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J. 21:2827–2832.
   PubMedGoogle Scholar
• Chen, B. P., D. W. Chan, J. Kobayashi, S. Burma, A. Asaithamby, K. Morotomi-Yano, E. Botvinick, J. Qin, and D. J. Chen. 2005. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem. 280:14709–14715.
   PubMed Web of Science ®Google Scholar
• Chen, B. P., N. Uematsu, J. Kobayashi, Y. Lerenthal, A. Krempler, H. Yajima, M. Lobrich, Y. Shiloh, and D. J. Chen. 2007. Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J. Biol. Chem. 282:6582–6587.
   PubMed Web of Science ®Google Scholar
• Chen, B. P., N. Uematsu, J. Kobayashi, Y. Lerenthal, A. Krempler, H. Yajima, M. Lobrich, Y. Shiloh, and D. J. Chen. 2006. ATM is essential for DNA-pkcs phosphorylations at T2609 cluster upon DNA double strand break. J. Biol. Chem. 282:6582–6587.
   PubMedGoogle Scholar
• Denekamp, J., G. F. Whitmore, and P. Jeggo. 1989. Biphasic survival curves for XRS radiosensitive cells: subpopulations or transient expression of repair competence? Int. J. Radiat. Biol. 55:605–617.
   PubMed Web of Science ®Google Scholar
• Difilippantonio, S., A. Celeste, M. J. Kruhlak, Y. Lee, M. J. Difilippantonio, L. Feigenbaum, S. P. Jackson, P. J. McKinnon, and A. Nussenzweig. 2007. Distinct domains in Nbs1 regulate irradiation-induced checkpoints and apoptosis. J. Exp. Med. 204:1003–1011.
   PubMed Web of Science ®Google Scholar
• Ding, Q., Y. V. Reddy, W. Wang, T. Woods, P. Douglas, D. A. Ramsden, S. P. Lees-Miller, and K. Meek. 2003. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. Mol. Cell. Biol. 23:5836–5848.
   PubMed Web of Science ®Google Scholar
• Douglas, P., G. P. Sapkota, N. Morrice, Y. Yu, A. A. Goodarzi, D. Merkle, K. Meek, D. R. Alessi, and S. P. Lees-Miller. 2002. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem. J. 368:243–251.
   PubMed Web of Science ®Google Scholar
• Falck, J., J. Coates, and S. P. Jackson. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605–611.
   PubMed Web of Science ®Google Scholar
• Gell, D., and S. P. Jackson. 1999. Mapping of protein-protein interactions within the DNA-dependent protein kinase complex. Nucleic Acids Res. 27:3494–3502.
   PubMed Web of Science ®Google Scholar
• Gellert, M. 2002. V(D)J. recombination: RAG proteins, repair factors, and regulation. Annu. Rev. Biochem. 71:101–132.
   PubMed Web of Science ®Google Scholar
• Goodarzi, A. A., Y. Yu, E. Riballo, P. Douglas, S. A. Walker, R. Ye, C. Harer, C. Marchetti, N. Morrice, P. A. Jeggo, and S. P. Lees-Miller. 2006. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J. 25:3880–3889.
   PubMed Web of Science ®Google Scholar
• Helleday, T., J. Lo, D. C. van Gent, and B. P. Engelward. 2007. DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair 6:923–935.
   PubMed Web of Science ®Google Scholar
• Lieber, M. R., H. Lu, J. Gu, and K. Schwarz. 2008. Flexibility in the order of action and in the enzymology of the nuclease, polymerases, and ligase of vertebrate non-homologous DNA end joining: relevance to cancer, aging, and the immune system. Cell Res. 18:125–133.
   PubMed Web of Science ®Google Scholar
• Ma, Y., U. Pannicke, K. Schwarz, and M. R. Lieber. 2002. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J. recombination. Cell 108:781–794.
   PubMed Web of Science ®Google Scholar
• Mari, P. O., B. I. Florea, S. P. Persengiev, N. S. Verkaik, H. T. Bruggenwirth, M. Modesti, G. Giglia-Mari, K. Bezstarosti, J. A. Demmers, T. M. Luider, A. B. Houtsmuller, and D. C. van Gent. 2006. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. USA 103:18597–18602.
   PubMed Web of Science ®Google Scholar
• Meek, K., S. Gupta, D. A. Ramsden, and S. P. Lees-Miller. 2004. The DNA-dependent protein kinase: the director at the end. Immunol. Rev. 200:132–141.
   PubMed Web of Science ®Google Scholar
• Modesti, M., M. S. Junop, R. Ghirlando, M. van de Rakt, M. Gellert, W. Yang, and R. Kanaar. 2003. Tetramerization and DNA ligase IV interaction of the DNA double-strand break repair protein XRCC4 are mutually exclusive. J. Mol. Biol. 334:215–228.
   PubMedGoogle Scholar
• Moshous, D., I. Callebaut, R. de Chasseval, B. Corneo, M. Cavazzana-Calvo, F. Le Deist, I. Tezcan, O. Sanal, Y. Bertrand, N. Philippe, A. Fischer, and J. P. de Villartay. 2001. Artemis, a novel DNA double-strand break repair/V(D)J. recombination protein, is mutated in human severe combined immune deficiency. Cell 105:177–186.
   PubMed Web of Science ®Google Scholar
• Ono, M., P. W. Tucker, and J. D. Capra. 1994. Production and characterization of recombinant human Ku antigen. Nucleic Acids Res. 22:3918–3924.
   PubMed Web of Science ®Google Scholar
• Riballo, E., M. Kuhne, N. Rief, A. Doherty, G. C. Smith, M. J. Recio, C. Reis, K. Dahm, A. Fricke, A. Krempler, A. R. Parker, S. P. Jackson, A. Gennery, P. A. Jeggo, and M. Lobrich. 2004. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16:715–724.
   PubMed Web of Science ®Google Scholar
• Rooney, S., J. Sekiguchi, C. Zhu, H. L. Cheng, J. Manis, S. Whitlow, J. DeVido, D. Foy, J. Chaudhuri, D. Lombard, and F. W. Alt. 2002. Leaky Scid phenotype associated with defective V(D)J. coding end processing in Artemis-deficient mice. Mol. Cell 10:1379–1390.
   PubMed Web of Science ®Google Scholar
• Singleton, B. K., M. I. Torres-Arzayus, S. T. Rottinghaus, G. E. Taccioli, and P. A. Jeggo. 1999. The C terminus of Ku80 activates the DNA-dependent protein kinase catalytic subunit. Mol. Cell. Biol. 19:3267–3277.
   PubMedGoogle Scholar
• Spagnolo, L., A. Rivera-Calzada, L. H. Pearl, and O. Llorca. 2006. Three-dimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol. Cell 22:511–519.
   PubMed Web of Science ®Google Scholar
• Stracker, T. H., M. Morales, S. S. Couto, H. Hussein, and J. H. Petrini. 2007. The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex. Nature 447:218–221.
   PubMedGoogle Scholar
• Uematsu, N., E. Weterings, K. Yano, K. Morotomi-Yano, B. Jakob, G. Taucher-Scholz, P. O. Mari, D. C. van Gent, B. P. Chen, and D. J. Chen. 2007. Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J. Cell Biol. 177:219–229.
   PubMed Web of Science ®Google Scholar
• van der Burg, M., N. S. Verkaik, A. T. den Dekker, B. H. Barendregt, I. Pico-Knijnenburg, I. Tezcan, J. J. vanDongen, and D. C. van Gent. 2007. Defective Artemis nuclease is characterized by coding joints with microhomology in long palindromic-nucleotide stretches. Eur. J. Immunol. 37:3522–3528.
   PubMedGoogle Scholar
• van Gent, D. C., J. H. Hoeijmakers, and R. Kanaar. 2001. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2:196–206.
   PubMed Web of Science ®Google Scholar
• van Gent, D. C., and M. van der Burg. 2007. Non-homologous end-joining, a sticky affair. Oncogene 26:7731–7740.
   PubMed Web of Science ®Google Scholar
• Verkaik, N. S., R. E. Esveldt-van Lange, D. van Heemst, H. T. Bruggenwirth, J. H. Hoeijmakers, M. Z. Zdzienicka, and D. C. van Gent. 2002. Different types of V(D)J. recombination and end-joining defects in DNA double-strand break repair mutant mammalian cells. Eur. J. Immunol. 32:701–709.
   PubMed Web of Science ®Google Scholar
• Walker, J. R., R. A. Corpina, and J. Goldberg. 2001. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412:607–614.
   PubMed Web of Science ®Google Scholar
• Wang, J., J. M. Pluth, P. K. Cooper, M. J. Cowan, D. J. Chen, and S. M. Yannone. 2005. Artemis deficiency confers a DNA double-strand break repair defect and Artemis phosphorylation status is altered by DNA damage and cell cycle progression. DNA Repair 4:556–570.
   PubMed Web of Science ®Google Scholar
• Weterings, E., and D. J. Chen. 2007. DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J. Cell Biol. 179:183–186.
   PubMed Web of Science ®Google Scholar
• Weterings, E., and D. J. Chen. 2008. The endless tale of non-homologous end-joining. Cell Res. 18:114–124.
   PubMed Web of Science ®Google Scholar
• Weterings, E., N. S. Verkaik, H. T. Bruggenwirth, J. H. Hoeijmakers, and D. C. van Gent. 2003. The role of DNA dependent protein kinase in synapsis of DNA ends. Nucleic Acids Res. 31:7238–7246.
   PubMed Web of Science ®Google Scholar
• Whitmore, G. F., A. J. Varghese, and S. Gulyas. 1989. Cell cycle responses of two X-ray sensitive mutants defective in DNA repair. Int. J. Radiat Biol. 56:657–665.
   PubMed Web of Science ®Google Scholar
• Yannone, S. M., I. S. Khan, R. Z. Zhou, T. Zhou, K. Valerie, and L. F. Povirk. 2008. Coordinate 5′ and 3′ endonucleolytic trimming of terminally blocked blunt DNA double-strand break ends by Artemis nuclease and DNA-dependent protein kinase. Nucleic Acids Res. 36:3354–3365.
   PubMedGoogle Scholar